This station is the southern terminal for J trains on weekends (from approximately 1 a.m. on Saturday to 5 a.m. on Monday) and during this time, they use the inner tracks to begin their return trip to Brooklyn and Queens.

The southbound platform is slightly higher at the southern end of the station because the next stop south, Fulton Street, is bi-level with the southbound platform being above the northern one.

The two "express" tracks at this station merge into a single tail track south of the station. The tail track is 620 feet long from the switch points to the bumper block, where an emergency exit is available.

North of this station, there are two stub tracks, which end behind the now-closed Queens-bound side platform.[4] These tracks were formerly connected to the Manhattan Bridge, until they were disconnected in 1967 as part of the Chrystie Street Connection.

Also north of this station, the former southbound express track (now the northbound track) splits into two tracks just south of Canal Street: the former northbound local track, and the former southbound express track (the current northbound track).

The tile work on this station includes a depiction of the nearby Brooklyn Bridge that suffers from an interesting gaffe: it features the parallel up-down cables between the main cable and the roadway (as seen alone on most suspension bridges) but misses the second set of diagonal cables that radiate from the bridge to the roadway (as seen on cable-stayed bridges).

This was one of the earliest BMT subway stations opened in New York City, built at a time when Lower Manhattan was the city's principal business district. It was designed to be the BMT's Manhattan hub, with trains arriving from Brooklyn in both directions, and terminating here. Originally, trains arrived from the north via either the Williamsburg Bridge or the Manhattan Bridge. The connection to the Montague Street Tunnel had not yet been completed.

The loop configuration permitted trains arriving in either direction from the BMT Fourth Avenue Line in Brooklyn to pass through Chambers Street and return to Fourth Avenue without having to reverse direction. A track connection to the Brooklyn Bridge, which would have made a similar loop through the Williamsburg Bridge, was planned in the station's design, but never built. (SeeBMT Brooklyn Loops.)

Although altered over the years to account for changing ridership patterns, the station has not been renovated. In one poll, it was voted the ugliest station in the system.[citation needed]

When it was being built before World War I, Chambers Street was envisioned as a City Hall terminal, a kind of downtown Grand Central at a time when the business and population center of the city was still closer to the southern end of the island. Three years after it opened, its four wide platforms were so overcrowded that one newspaper article described them as more dangerous during the rush hours than at the Grand Central or the Fourteenth Street Stations.

But by the mid-1920s, the subway itself was pushing the city's population north and leaving Chambers Street behind. By as early as the 1930s, in fact, the station's ridership had dropped off so steeply that half of it was closed.

By the 1950s, many of the city's business interests had shifted to Midtown. The Chrystie Street Connection, completed in 1967, severed the Nassau line's connection to the Manhattan Bridge, so that the bridge tracks could connect instead to the uptown IND Sixth Avenue Line. The tracks heading towards the Manhattan Bridge (now used for train storage) are visible from northbound trains leaving Chambers Street.

The tail track south of the station was the site of a R42 crash into the bumper block on the lower level relay track on November 6, 2007. The train was operating on the M service when it crashed.[5]

Just north of the station are crossovers that allow trains to switch between the local and express tracks, which allow Lexington Avenue local trains to continue south via the express tracks if necessary (rather than using the City Hall loop). Due to the closure of City Hall station in 1945, Brooklyn Bridge – City Hall (which had simply been Brooklyn Bridge) became the southernmost station on normal Lexington Avenue local service.

South of the station, the downtown local track splits into three tracks. The westernmost track loops around to the northbound local track through City Hall station. The other two are layup tracks parallel to the downtown express track. Until the 1960s, they merged into the downtown express track north of Fulton Street, but now they end at bumper blocks a little north of Fulton Street, and are occasionally used for train storage.

The station has been renovated, with new tile and ADA-accessible elevator access. It is the zero point for the IRT East Side chain; mile 0 is at the south end of the station.

The Brooklyn Bridge station has a number of closed off areas as construction and service patterns have required changes to be made to the station. In addition to the two island platforms, there are two short side platforms on the outer edges of the station. Like those on the IRT Lexington Avenue Line at 14th Street – Union Square and on the IRT Broadway – Seventh Avenue Line at 96th Street, these side platforms were built to accommodate extra passenger volume and were built to the five-car length of the original IRT local trains. These platforms did not see much use as they were located at express stations, which allows cross-platform interchanges via the island platforms. When trains were lengthened to their current ten-car length, it was impractical to lengthen both these side platforms and the island platforms. They were closed in 1910 after only six years in operation and walled off along the platform edges.

The side platform on the southbound side is now home to some electrical equipment and a backup control tower for the Brooklyn Bridge interlocking, just north of the station. The tower is functional but not normally used, because the Grand Central – 42nd Street tower is the primary control point for the whole line. The interlocking board can be seen through a window along the wall along the southbound local trackway. The south end of the downtown side platform is still visible near the dispatcher's booth on the downtown island platform.

There are also some closed portions at the south ends of the existing express platforms. During the station lengthening projects it was easier to lengthen the express platform to the north. The curves at the south end proved impossible to rework so the station was lengthened northward (allowing Worth Street to be closed), and the curved southern ends of the express platform closed. Gap fillers and original mosaic tiles remain in the closed ends.